CYTOTAXONOMY OF SHREWS OF THE GENUS CROCIDURA FROM MEDITERRANEAN ISLANDS

HAL Id: hal-03035858

https://hal.archives-ouvertes.fr/hal-03035858

HAL is a multi-disciplinary open access archive for the deposit and dissemination of sci-entific research documents, whether they are pub-lished or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

CYTOTAXONOMY OF SHREWS OF THE GENUS

CROCIDURA FROM MEDITERRANEAN ISLANDS

P Vogel, T Maddalena, P Schembri

To cite this version:

P Vogel, T Maddalena, P Schembri. CYTOTAXONOMY OF SHREWS OF THE GENUS CRO-CIDURA FROM MEDITERRANEAN ISLANDS. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 1990, pp.124-129. �hal-03035858�

CYTOTAXONOMY OF SHREWS OF THE GENUS CROCIDURA

FROM MEDITERRANEAN ISLANDS

P. VOGEL

, T. MADDALENA

, P.J. SCHEMBRI

1 Institut de Zoologie et d'Ecologie Animale, Université de Lausanne, CH-1015 Lausanne, Suisse 2 Department of Biology, University of Malta, Msida, Malta

SORICIDAE CROCIDURA TAXONOMŒ BIOGÉOGRAPHIE

RÉSUMÉ - Il a été possible de vérifier le statut taxonomique de diverses popu-lations de Musaraignes insulaires grâce à l'étude chromosomique. Quatre espèces ont été mises en évidence par cette méthode. Deux espèces, C. russula et C. sua-veolens, sont d'origine continentale, introduites sur les îles par l'homme. En re-vanche, pour deux autres espèces, C. sicula de Sicile et de Gozo et C. zimmermanni de Crète, aucune population continentale n'est connue et il faut les considérer comme survivantes des faunes insulaires du Pléistocène.

SORICIDAE CROCIDURA TAXONOMY BIOGEOGRAPHY KARYOTYPE

ABSTRACT - Thanks to chromosome studies it was possible to review the tax-onomic status of many insular populations of shrews and to demonstrate the pré-sence of four distinct species. Two of thèse, C. russula and C. suaveolens, are of continental origin and have been introduced on the islands by man. On the con-trary, the other two species, C. sicula from Sicily and Gozo, and C. zimmermanni from Crète, are not known from continental land masses and we consider them to be survivors from the insular faunas of the Pleistocene.

INTRODUCTION

According to the list compiled by Ellerman and Morrison-Scott (1966), 27 species of the genus

Crocidura have been described from Europe. Most

of thèse are local forms and modem taxonomists like Jenkins (1976) and Corbet (1978) recognize only three valid species : C. leucodon, C. russula and C. suaveolens. This discrepancy is due to the fact that thèse species are morphologically very similar whereas intraspecific variability is rather high. The taxonomic assignment of island popu-lations is particularly problematic as morphology is strongly affected by genetic isolation and the particular sélective pressures of island environ-ments. The history of the taxonomic interprétation of the shrews of Crète provides a good illustration (Table 1).

When morphological interprétations remain un-certain, other techniques are needed. One of the most effective is détermination of the karyotype, which, in the genus Crocidura, is very différent between species, but shows minimal intraspecific variation (Reumer and Meylan 1986). As the three

continental species of Crocidura have distinct karyotypes (Fig. 1), this method was systemati-cally applied to island populations in an effort to résolve their taxonomy. The results of thèse stu-dies have been published in many scattered pub-lications and it is useful therefore to présent a synthetic review. Four of the five European spe-cies here recognized are documented with pictures of the living animais (Fig. 2). A map of the Medterranean région showing the geographical

Table I. - The history of the taxonomic interprétation of the shrews of Crète based on morphological analyses.

Author Lowland form Mountain form Miller 1909 C. caneae

Bace 1913 C. (russula) caneae

Wectstein 1953 C. russula caneae C. russula zimmermanni

Richter 1970 C. gueldenstaedtii C. russula zimmermanni

Vesmanis & Kahmann C. gueldenstaedtii C. zimmermanni*

(1978)

CROCIDURA FROM MEDITERRANEAN ISLANDS 125

A*—

XX

If

-

**"

B

~j

||~Wl

MA Si

HPinfcir

S

«r

01 1*

n A m

**

Fig. 1. - Karyotypes of the European species of the genus Crocidura. NF is the number of chromosome arms in the female.

Fig. 2. - A. C. russula (from Switzerland), B. C. suaveolens (from Corsica), D. C. sicula (from Gozo), D. C. leucodon (from Georgia, USSR). No photographs of living C. zimmermanni exist.

Fig. 3. — Distribution of Crocidura spp. on Mediterranean islands as determined by chromosomal and biochemical

analyses. Islands : 1 = Ibiza, 2 = Minorca, 3 = Corsica, 4 = Sardinia, 5 = Sicily, 6 = Gozo, 7 = Crète, 8 = Cyprus.

distribution of the karyologically determined populations is also given (Fig. 3).

MATERIAL AND METHODS

The source of the material which served for chromosomal analysis (carried out either in Lausanne or in Montpellier) is as follows : Cor-sica : R. Fons (Banyuls, F); Crète : M. Geiger & R Vogel (Lausanne, CH); Cyprus and Lesbos : F. Catzeflis & C. Doerig (Lausanne); Gozo : RJ. Schembri, M. Borg (Malta) & P. Vogel (Lausanne); Ibiza and Minorca : F. Poitevin (Montpellier, F); Sardinia : A. Geraets & R. Hutterer (Bonn, D.); Sicily : P. Vogel (Lausanne).

In some cases the karyotypes were prepared directly in the field. Two techniques were em-ployed, either the squash method using fragments of the spleen (Meylan 1967) or the air-drying tech-nique using bone marrow (Baker et al. 1982). In order to study other parameters from the same shrews, laboratory breeding populations were es-tablished when possible.

island. According to an analysis of owl pellets by F. Poitevin (pers. comm.) two species may occur on Lesbos.

Crocidura russula (Hermann, 1780)

Greater white-toothed shrew. According to Jenkins (1976) and Corbet (1978), this species oc-curs from the Near East (Israël, Turkey), through Middle and South Europe, to North Africa. By means of cytotaxonomy it was possible to show its absence south of the Alps (Meylan and Hausser 1974) and to demonstrate that the populations from eastern Europe and the Near East assigned to this species in fact ail belong to C. suaveolens (Catzeflis et al. 1985). Thus the continental dis-tribution of C. russula is limited to parts of Cen-tral and southwestern Europe, as well as to North Africa, its probable place of origin (Catzeflis 1984, Vogel and Maddalena 1987). On Mediter-ranean islands C. russula occurs only on Sardinia (Catzeflis 1983) and Ibiza (Catalan et al. 1988). According to Sans-Coma et al. (1985) and Vigne and Alcover (1985) it was introduced during his-torical times.

DISTRIBUTION OF THE SPECIES

Crocidura leucodon (Herman, 1780)

Bicoloured white-toothed shrew. This shrew may occur on Lesbos, Greece (two spécimens as-signed by Ondrias, 1969, to C. lasiura), but Catze-flis et al. (1985) found only C. suaveolens on this

Crocidura suaveolens (Pallas, 1811)

Lesser white-toothed shrew. This species orig-inates in Asia (Catzeflis 1984) but now occupies a wide distributional range from Portugal to Korea (Corbet 1978). In North Africa, C. whitakeri was previously considered to be a subspecies of C.

CROCIDURA FROM MEDITERRANEAN ISLANDS 127

suaveolens, but this interprétation is no longer

ac-ceptée! (Hutterer 1986, Rzebik-Kowalska 1988). However, Vesmanis (1988) recently assigned one skull of Tunisian origin to C. suaveolens. Because of the uncertain taxonomic value of teeth charac-ters, a cytogenetic investigation of Crocidura of the North African région is needed.

Populations of the Near East still présent a tax-onomic problem. Russian authors (Gureev 1971, Tembotova 1983, Grafodatskii et al. 1988) con-sider them as a separate species, C. gueldenstaedtii (Pallas, 1811). Their interprétation is based on morphological variations, whereas the karyotype is absolutely identical to that of C. suaveolens (Catzeflis et al. 1985, Tembotova 1987, Grafodat-skii et al. 1988). Considering the interfertility be-tween suaveolens and gueldenstaedtii (Catzeflis et

al. 1985), the absence of sympatry (Zaitsev in litt.)

and their close biochemical relationship (Mad-dalena 1990), we include ail thèse populations in the species C. suaveolens.

The présence of C. suaveolens on the following islands was confirmed by cytotaxonomy : Cyprus and Lesbos (Catzeflis 1983, Catzeflis et al. 1985), Corsica (Catalan 1984, Poitevin et al. 1986), Minorca (Catalan et al. 1988), Crète (Vogel et al. 1986). In ail cases this species was most probably introduced by man. In the case of Crète this was most probably during the Minoan period, about l'500 BC (Reumer and Payne 1986). The bio-chemical similarity of Cretan populations with those from Turkey reveals the origin of this island population (Vogel et al. 1986). On Minorca C.

suaveolens arrived about 200 BC (Vigne and

Al-cover 1985). On Corsica its présence was at first documented only from the Middle Ages (Vigne and Alcover 1985), however new findings provide évidence of a much earlier introduction (Vigne and Marinval-Vigne, in press).

Crocidura sicula Miller, 1901

Crocidura zimmermanni Wettstein, 1953

Zimmermann's shrew. This shrew was origi-nally described as a subspecies of C. russula. Based on morphological criteria, Vesmanis and Kahmann (1978) raised this taxon to species rank. The validity of this interprétation was confirmed by the particular karyotype (Vogel 1986). Fossils of this species, together with others of Kritimys, have been found in karst fissures infilled with Pleistocene sédiments (Reumer 1986). To day, this shrew is not known from anywhere outside Crète and it is therefore considered endémie to this is-land. Its numerical dominance in the mountains and its absence in the fertile plains of the island (Vogel et al. 1986, Pieper in press) are probably the conséquence of direct compétition with the in-vading C. suaveolens.

CONCLUSIONS

Thanks to cytogenetic methods, the systematic status of the shrews of many Mediterranean is-lands has now been clarified. This has not been without surprising results. In some cases, previous morphological interprétations have been con-firmed, e.g. that of Vesmanis and Kahmann (1978) concerning Zimmermann's shrew, at the same time resolving such complex problems as the uncertain interprétation of Miller's type spécimens from Sic-ily. In other cases, previous morphological inter-prétations have been shown to be wrong as, for example, those of ail former authors dealing with the shrews of Gozo. The présent state of our knowledge gives a solid basis for further zoogeo-graphical investigations which, sustained by bio-chemical techniques, can help to détermine the genetic relationship between populations and thus, together with palaeontology and archaeology, allow a reconstruction of the exciting history of island colonization.

Sicilian shrew. It is only with the cytogenetic analysis of shrews from Sicily (Vogel 1988) and from Gozo that it became clear that ail the

Crocidura from the Siculo-Maltese archipelago,

earlier variously assigned to C. caudata, C.

leu-codon, C. russula, C. sicula and C. suaveolens,

actually belong to the same species, C. sicula (Vogel et al. 1989). Many indications provide con-vincing arguments that this shrew is a survivor from the Pleistocene (Hutterer, in press). The strong genetical relationship between C. sicula and

C. canariensis (Maddalena and Vogel, in press)

in-dicates that thèse two species are closely related. Their relationship with the so far unkaryotyped North African species needs further investigation.

BIBLIOGRAPHY

BATE D.M.A., 1913. The mammals of Crète. In Trevor Battye : A camping in Crète. London.

BAKER R.J., N.W. HAIDUK, L.W. ROBBINS, A. CADENA & B.F. KOOP, 1982. Chromosomal studies of South American bats and their systematic impli-cations. Spécial. Publ. Pymatuning Lab. Ecol. 6 : 303-327.

CATALAN J., 1984. Méthodes génétiques appliquées à la systématique des Soricidae du Midi de la France. Diplôme EPHE, Montpellier.

CATALAN J., F. POITEVIN, R. FONS, S. GUER-ASIMOV & H. CROSET, 1988. Biologie évolutive

CATZEFLIS F, 1983. Analyse cytologique et bio-chimique des Crocidures de l'île de Chypre (Mam-malia, Insectivora). Rev. suisse Zool. 90 : 407-415. CATZEFLIS F., 1984. Systématique biochimique,

tax-onomie et phylogénie des Musaraignes d'Europe (Soricidae, Mammalia). Thèse, Univ. Lausanne, Suisse.

CATZEFLIS F., T. MADDALENA, S. HELLWING & P. VOGEL, 1985. Unexpected findings on the tax-onomic status of East Mediterranean Crocidura

russula auct. (Mammalia, Insectivora). Z. Sàugetierk. 50 : 185-201.

ELLERMAN J.R. & T.C.S. MORRISON-SCOTT, 1966. Checklist of Palaearctic and Indian mammals, 1758 to 1946. 2d. Trustées Brit. Mus (Nat. Hist) London. CORBET G.B., 1978. The mammals of the Palaearctic région : a taxonomic review. Brit. Mus. (Nat. Hist.), Cornell Univ. Press, London.

GRAFODATSKY A.S., S.I. RADZHABLI, A.V. SHAR-SHOV & M.V ZAITSEV, 1988. Karyotypes of five

Crocidura species of the USSR Fauna. Tsytologiva

(in Russian) 30 : 1247-1255.

GUREV A.A., 1971. Shrews (Soricidae) of the world fauna. Leningrad (in Russian).

HUTTERER R., 1981. Der Status von Crocidura

ari-adne Pieper, 1979 (Mammalia : Soricidae). Bonn, zool. Beitr. 32 : 3-12.

HUTTERER R., 1986. The species of Crocidura (Sori-cidae) in Morocco. Mammalia 50 : 521-534. HUTTERER R., 1990. Temporal and geographical

var-iation of shrews of the Sicilian-Maltese archipelago since the Pleistocene. Vie Milieu 40 (2/3) :.

JENKINS P.D., 1976. Variation in Eurasian shrews of the genus Crocidura (Insectivora : Soricidae). Bull.

Brit. Mus. (Nat. Hist.) Zool. 30 : 271-309.

MADDALENA T., 1990. Systématique, évolution et bi-ogéographie des musaraignes Paléarctiques et Afrotropicales de la sous-famille des Crocidurinae : une approche génétique.Thèse, Univ. Lausanne, Suisse.

MADDALENA T. & P. VOGEL. Relations génétiques entre Crocidures méditerranéennes : le cas des musaraignes de Gozo (Malte). Vie Milieu 40 (2/3) MEYLAN A., 1967. Formules chromosomiques et

pol-ymorphisme robertsonien chez Blarina brevicauda (Say) (Mammalia : Insectivora). Can. J. Zool. 45 : 1119-1127.

MEYLAN A. & J. HAUSSER, 1974. Position cytotax-onomique de quelques musaraignes du genre

Crocidura au Tessin (Mammalia, Insectivora). Rev. suisse Zool. 81 : 701-710.

MILLER G.S., 1909. Twelve new European mammals.

Ann. Mag. nat. hist., Ser. 8, 3 : 415-422.

ONDRIAS J., 1969. Die Ussuri-Gross-Spitzmaus,

Crocidura lasiura Dobson, 1890, auf der Aegàischen

Insel Lesbos. Z. Sàugetierk. 34 : 353-358.

POITEVIN F, J. CATALAN, R. FONS et H. CROSET 1986. Biologie évolutive des populations ouest-européennes de crocidures. I. Critères d'identifica-tion et répartid'identifica-tion biogéographique de Crocidura

russula (Hermann, 1780) et Crocidura suaveolens

(Pallas 1811). Rev. Ecol. (Terre Vie) 41: 299-314. REUMER J.W.F., 1986. Notes on the Soricidae

(Insec-tivora, Mammalia) from Crète. I. The Pleistocene species Crocidura zimmermanni. Bonn. zool. Beitr.

37: 161-171.

REUMER J.W.F. & A. MEYLAN, 1986. New develop-ments in vertebrate cytotaxonomy IX, Chromosome numbers in the order Insectivora (Mammalia).

Genet-ica 70 : 119-151.

REUMER J.W.F. & S. PAYNE, 1986. Notes on the Sori-cidae (Insectivora, Mammalia) from Crète II. The shrew remains from Minoan and Classical Kommos.

Bonn. zool. Beitr. 37: 173-182.

RICHTER H., 1970. Zum taxonomischen Status der zwei Crocidura-Formen von Kreta (Mammalia, In-sectivora, Soricidae). Zool. Abh. Mus. Tierk. Dresden

31: 279-291.

RZEBIK-KOWALSAKA B., 1988. Studies on the genus

Crocidura (Insectivora, Mammalia) in Algeria. Acta Zool. Cracov. 31 : 167-192.

SANS-COMA V, J.A. ALCOVER & MJ. LOPEZ-FUSTER, 1985. Morphometrischer Vergleich re-zenter und subfossiler Etruskerspitzmâuse Suncus

etruscus (Savi, 1822) von der Insel Sardinien. Sàugetierkdl. Mitt. 32 : 151-158.

TEMBOTOVA F.A., 1983. Taxonomic weight of some features of Crocidura species from Caucasus. In : the population variability of the species and the problem of protection of the génotypes of mammals. Acad. Sci. USSR, 125-127 (in Russian).

TEMBOTOVA F.A., 1987. Systematics of white-toothed shrews from Caucasus. In : Fauna and ecology of mammals from Caucasus. ed. Tembotov, A.K., H.H. Tchaschamifchev, T. Totchiev & L.V. Milanova. Nal'chik (in Russian).

VESMANIS LE., 1988. Ein Nachweis der Gartenspitz-maus, Crocidura suaveolens (Pallas, 1811), in Tune-sien (Mammalia, Insectivora, Soricidae). Zool.

Abhandl. Staat. Mus. Tierk. Dresden 44 : 75-82.

VESMANIS I. & H. KAHMANN, 1978. Mor-phometrische Untersuchungen an Wimperspitz-mâusen (Crocidura). 4. Bemerkungen tiber die Typusreihe der kretaischen Crocidura russula zimmermanni Wettstein, 1953 im Vergleich mit Crocidura gueldenstaedti caneae (Miller, 1909). Sàugetierkdl. Mitt. 40 : 214-222.

VIGNE D. & A. ALCOVER, 1985. Incidence des rela-tions historiques entre l'homme et l'animal dans la composition actuelle du peuplement amphibien, rep-tilien et mammalien des îles de Méditerranée oc-cidentale. 110e Congr. nat. Soc. sav., Montpellier,

CROCIDURA FROM MEDITERRANEAN ISLANDS 129

VIGNE J.D. & M.C. MARINVAL-VIGNE, 1990. Nou-velles données sur l'histoire des Insectivores Sori-cidés en Corse. Vie Milieu 40 (2/3).

VOGEL P., 1986. Der Karyotyp der Kretaspitzmaus

Crocidura zimmermanni Wettstein, 1953 (Mammalia,

Insectivora). Bonn. zool. Beitr. 37 : 35-38.

VOGEL P., 1988. Taxonomical and biogeographical problems in Mediterranean shrews of the genus

Crocidura (Mammalia, Insectivora) with référence to

a new karyotype from Sicily (Italy). Bull. Soc. vaud.

Sci. nat. 79 : 39-48.

VOGEL P., R. HUTTERER & M. SARA, 1989. The cor-rect name, species diagnosis and distribution of the Sicilian shrew. Bonn. zool. Beitr. 40 : 243-248.

VOGEL P., T. MADDALENA & F. CATZEFLIS, 1986. A contribution to the taxonomy and ecology of shrews (Crocidura zimmermanni and C. suaveolens) from Crète and Turkey. Acta Theriol. 31 : 537-545. VOGEL P. & T. MADDALENA, 1987. Note sur la rép-artition altitudinale et la fréquence de la musaraigne musette (Crocidura russula yebalensis) au Maroc.

Mammalia 51 : 465-467.

WETTSTEIN O., 1953. Die Insectivora von Kreta. Z.

Sàugetierk. 17 : 4-13.

Reçu le 14 novembre 1989; received November 14, 1989 Accepté le 12 janvier 1990; accepted January 12, 1990